Elastic Properties of Active Muscle-On the Rebound?

Monroy, Jenna A.; Lappin, A. Kristopher; Nishikawa, Kiisa C.

doi:10.1097/jes.0b013e318156e0e6

Cited by 28 publications

(32 citation statements)

References 25 publications

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“…The steady-state force produced by muscles after active shortening is less than the isometric force at a corresponding length, and likewise the steady-state force following active lengthening is higher than the isometric force at a corresponding length. These history-dependent properties of active muscle are exactly those expected of springs, which produce greater tensile force when stretched and less tensile force when shortened, in proportion to their change in length [78].…”

Section: Explanatory Value Of the Winding Filament Modelmentioning

confidence: 58%

Is titin a ‘winding filament’? A new twist on muscle contraction

et al. 2011

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Recent studies have demonstrated a role for the elastic protein titin in active muscle, but the mechanisms by which titin plays this role remain to be elucidated. In active muscle, Ca 2þ -binding has been shown to increase titin stiffness, but the observed increase is too small to explain the increased stiffness of parallel elastic elements upon muscle activation. We propose a 'winding filament' mechanism for titin's role in active muscle. First, we hypothesize that Ca 2þ -dependent binding of titin's N2A region to thin filaments increases titin stiffness by preventing low-force straightening of proximal immunoglobulin domains that occurs during passive stretch. This mechanism explains the difference in length dependence of force between skeletal myofibrils and cardiac myocytes. Second, we hypothesize that cross-bridges serve not only as motors that pull thin filaments towards the M-line, but also as rotors that wind titin on the thin filaments, storing elastic potential energy in PEVK during force development and active stretch. Energy stored during force development can be recovered during active shortening. The winding filament hypothesis accounts for force enhancement during stretch and force depression during shortening, and provides testable predictions that will encourage new directions for research on mechanisms of muscle contraction.

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Section: Explanatory Value Of the Winding Filament Modelmentioning

confidence: 58%

Is titin a ‘winding filament’? A new twist on muscle contraction

et al. 2011

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“…During load-clamp experiments, muscles are rapidly unloaded while the change in muscle length is recorded. When the load is reduced, muscles shorten biphasically, with an initial rapid change in length owing to recoil of elastic elements and a later slow phase due to cross-bridge cycling (Wilkie, 1956;Jewell and Wilkie, 1958;Lappin et al, 2006;Monroy et al, 2007). For each muscle, the initial stress and change in stress were matched for load-clamps in the active and passive states (Fig.…”

Section: Elastic Propertiesmentioning

confidence: 99%

Effects of activation on the elastic properties of intact soleus muscles with a deletion in titin

Monroy

Powers

Pace

et al. 2016

Journal of Experimental Biology

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Titin has long been known to contribute to muscle passive tension. Recently, it was also demonstrated that titin-based stiffness increases upon Ca 2+ activation of wild-type mouse psoas myofibrils stretched beyond overlap of the thick and thin filaments. In addition, this increase in titin-based stiffness was impaired in single psoas myofibrils from mdm mice, characterized by a deletion in the N2A region of the Ttn gene. Here, we investigated the effects of activation on elastic properties of intact soleus muscles from wild-type and mdm mice to determine whether titin contributes to active muscle stiffness. Using load-clamp experiments, we compared the stress-strain relationships of elastic elements in active and passive muscles during unloading, and quantified the change in stiffness upon activation. Results from wild-type muscles show that upon activation, the elastic modulus increases, elastic elements develop force at 15% shorter lengths, and there was a 2.9-fold increase in the slope of the stress-strain relationship. These results are qualitatively and quantitatively similar to results from single wild-type psoas myofibrils. In contrast, mdm soleus showed no effect of activation on the slope or intercept of the stress-strain relationship, which is consistent with impaired titin activation observed in single mdm psoas myofibrils. Therefore, it is likely that titin plays a role in the increase of active muscle stiffness during rapid unloading. These results are consistent with the idea that, in addition to the thin filaments, titin is activated upon Ca 2+ influx in skeletal muscle.

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“…Phosphorylation (Hidalgo et al, 2009;Krüger et al, 2009), small heat shock protein infiltration (Kötter et al, 2014) and disulfide bonding (Alegre-Cebollada et al, 2014) are among the many processes by which the stiffness of I-band titin can be modulated to protect the protein from damage during stretch. While the contribution of titin-based stiffness to muscle force has traditionally been limited to passive stretch, this conventional view of titin is now being challenged with numerous studies which also demonstrate tuning of the spring properties of titin during calcium activation (Tatsumi et al, 2001;Campbell and Moss, 2002;Labeit et al, 2003;Bianco et al, 2007;Monroy et al, 2007;. The configuration of the extensible I-band of titin is changed in the presence of calcium (Tatsumi et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Titin force is enhanced in actively stretched skeletal muscle

Powers

Schappacher‐Tilp

Jinha

et al. 2014

Journal of Experimental Biology

131

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The sliding filament theory of muscle contraction is widely accepted as the means by which muscles generate force during activation. Within the constraints of this theory, isometric, steady-state force produced during muscle activation is proportional to the amount of filament overlap. Previous studies from our laboratory demonstrated enhanced titin-based force in myofibrils that were actively stretched to lengths which exceeded filament overlap. This observation cannot be explained by the sliding filament theory. The aim of the present study was to further investigate the enhanced state of titin during active stretch. Specifically, we confirm that this enhanced state of force is observed in a mouse model and quantify the contribution of calcium to this force. Titin-based force was increased by up to four times that of passive force during active stretch of isolated myofibrils. Enhanced titin-based force has now been demonstrated in two distinct animal models, suggesting that modulation of titin-based force during active stretch is an inherent property of skeletal muscle. Our results also demonstrated that 15% of the enhanced state of titin can be attributed to direct calcium effects on the protein, presumably a stiffening of the protein upon calcium binding to the E-rich region of the PEVK segment and selected Ig domain segments. We suggest that the remaining unexplained 85% of this extra force results from titin binding to the thin filament. With this enhanced force confirmed in the mouse model, future studies will aim to elucidate the proposed titin-thin filament interaction in actively stretched sarcomeres.

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Elastic Properties of Active Muscle-On the Rebound?

Cited by 28 publications

References 25 publications

Is titin a ‘winding filament’? A new twist on muscle contraction

Is titin a ‘winding filament’? A new twist on muscle contraction

Effects of activation on the elastic properties of intact soleus muscles with a deletion in titin

Titin force is enhanced in actively stretched skeletal muscle

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